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Anopheles Arabiensis Behaviour and Ecology for the Dissemination of Pyriproxyfen, a Novel Technique for Malaria Vector Control in Tanzania

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Exploitation of adult Anopheles arabiensis behaviour and ecology for the dissemination of pyriproxyfen, a novel technique for malaria vector control in Tanzania Dickson Wilson Lwetoijera Thesis submitted in accordance with the requirements of the University of Liverpool for the degree of Doctor of Philosophy January 2016 1 ABSTRACT Effective larviciding to manage mosquito aquatic habitats offers an additional strategy for malaria vector control by complementing benefits already achieved by long lasting insecticide- treated nets (LLINs) and indoor residual spraying (IRS). Sustainable implementation of larviciding requires comprehensive understanding of the ecology of disease vectors and robust monitoring of factors governing local disease transmission. Treatment of aquatic habitats with the juvenile hormone analogue Pyriproxyfen (PPF), inhibits adult mosquito emergence at extremely low concentrations that are potentially deliverable by PPF-contaminated gravid adult females, a phenomenon termed „autodissemination‟. The primary aim of this thesis was to investigate a range of adult mosquito behaviours that might be exploited to disseminate PPF. The effectiveness of PPF to sterilize adult mosquitoes for malaria vector control was also assessed in a controlled system. Vector dynamics, malaria transmission intensity and risk factors were evaluated at the field site where the PPF autodissemination strategy would be evaluated in field trials and potentially implemented. Field monitoring of indoor malaria transmission risk factors revealed that even in the communities with high coverage of bednets, LLINs did not reduce the indoor densities of An. gambiae s.l (RR= 0.74 (0.50 - 1.11, p > 0.05) but reduced An. funestus indoor densities by 56% (RR= 0.44 (0.23 - 0.87, p < 0.05)). Houses with eave gaps had 3.3 and 5.5 times more An. gambiae s.l. (RR= 3.3 (2.39 - 4.56, p < 0.05)) and An. funestus ((RR = 5.55 (3.25 - 9.46, p < 0.05)) respectively. Intact screening over windows reduced up to 66% (RR = 0.34 (0.17 - 0.69)) and 83% (RR = 0.17 (0.08 - 0.39)) indoor entry of An. gambiae s.l. and An. funestus respectively. Furthermore, surveillance of wild malaria vectors populations and susceptibility to insecticide resistance demonstrated significant increase in An. funestus densities in 2012 (RR=1.56 (1.33- 1.69)) compared to An.gambiae s.l. (p <0.0001). In 2014, the proportion of An. gambiae s.l. catches (67%; 4373/6373) was higher than An. funestus (33%; 2100/6373). PCR results revealed change in relative proportion between the two sibling species of An.gambaie s.l. with a significant decrease in An. gambiae s.s. from approximately 14% (414/2,924) in 2008 to 0% (0/435) in 2014. Insecticide susceptibility tests indicated high resistance in An. funestus against deltamethrin (mortality rate in discriminating dose assay = 87%), lambda cyhalothrin (74%), permethrin (65%), bendiocarb (65%), and DDT (66%). Similarly, An. arabiensis showed insecticide resistance to permethrin (77%), deltamethrin (64%) and lambda cyhalothrin (42%) in 2014. In large screened cages it was demonstrated that adult An. arabiensis can disseminate PPF from clay pots treated with PPF to the aquatic habitats, resulting in 76.5% reduction in adult emergence, with higher mean proportion of adult emerging from untreated chamber, 0.95 (0.56 - 1.34) compared to the treated chamber, 0.21 (0.09 - 0.51, p < 0.0001). Treatment of a single clay pot resulted in 58% reduction in adult emergence in six habitats, with mean proportion of 0.34 (0.21 – 0.45) compared to the controls, 0.98 (0.96 – 1.00, p < 0.0001), showing a high level of habitats coverage amplification of the autodissemination event. After treating the walls and ceilings of cattle shelters with PPF, mosquito sterilization resulted in > 95% (89.3 - 102.9%) reduction in adult An. arabiensis production. This research provides evidence on the need of better housing and larviciding to complement LLINs in controlling the remaining malaria transmission transmitted by An. funestus and An. arabiensis. It also demonstrated for the first time that the PPF autodissemination strategy and sterilization of adult females present a promising malaria vector control option for field trial. PPF-autodissemination can be integrated into a vector management toolbox to control outdoor malaria transmission and also target multiple disease-carrying mosquitoes that share aquatic habitats with malaria vectors. These findings highlight the potential of PPF for controlling outdoor and indoor malaria vectors and call for further testing in the field. 2 DECLARATION I declare that this thesis is my own original work and that none of the material in this thesis has been presented or submitted to any other University for a similar degree award. Chapters 2, 3, 4 and 5 have already been published as reports in peer-reviewed journals, as Lwetoijera et al. and are presented in this thesis with minimal modification. Since those publications had multiple authors, the individual contributions of the co- authors are described here:- Chapter 2: A need for better housing to further reduce indoor malaria transmission in areas with high bed net coverage. Dickson W. Lwetoijera (DWL) proposed the study, supervised field data collection, analysed the data and drafted the manuscript under the supervision of Silas Majambere (SM), Samson K. Kiware (SSK) and Brian Faragher (BF) assisted in data analysis. The additional authors, Zawadi D. Mageni (ZDM), Caroline Harris (CH), Stefan Dongus (SD) and Gregor J. Devine (GJD), contributed to and approved the final manuscript. Chapter 3: Increasing role of Anopheles funestus and Anopheles arabiensis in malaria transmission in the Kilombero Valley, Tanzania. DWL conceived the study hypothesis, designed and supervised data collection, performed data analysis and drafted the manuscript under supervision of SM and Philip J. McCall (PJM). CH, SSK, SD and GJD contributed to the study design, and contributed to and approved the final manuscript. Chapter 4: Effective autodissemination of pyriproxyfen to breeding sites by the exophilic malaria vector Anopheles arabiensis in semi-field settings in Tanzania. DWL, SM and GD conceived the study hypothesis. DWL developed the study protocols and conducted the experiments; DWL, SSK and CH performed statistical analysis and interpreted the results. SM and PJM supervised the experimental progress and 3 supervised drafting of the manuscript. All authors contributed to and approved the final manuscript. Chapter 5: Comprehensive sterilization of resilient malaria vectors: a step closer to malaria elimination. DWL and SM conceived the study hypothesis, summarized and analysed the data under guidance of SSK and CH, and wrote the first manuscript draft. DWL prepared the study protocols, and performed and supervised the experiments under supervision of SM and PJM. All authors contributed to and approved the final manuscript. All remaining parts of the thesis were written by DWL, under the guidance of PJM and SM. Signed :................................................(Candidate) Date:.................................................... 4 TABLE OF CONTENTS ABSTRACT ....................................................................................................................... 2 DECLARATION ............................................................................................................... 2 TABLE OF CONTENTS ................................................................................................... 5 ACKNOWLEDGMENTS ................................................................................................. 9 LIST OF TABLES ........................................................................................................... 11 LIST OF FIGURES ......................................................................................................... 12 LIST OF ABBREVIATIONS .......................................................................................... 14 1 INTRODUCTION AND LITERATURE REVIEW .......................................... 16 1.1 Malaria ................................................................................................................ 16 1.1.1 Malaria parasites and transmission ............................................................ 17 1.1.2 Malaria vectors ........................................................................................... 20 1.1.3 Biology of the main African anopheline vectors ....................................... 21 1.2 Control of malaria vectors and challenges to existing approaches ..................... 23 1.2.1 Integrated vector management ................................................................... 25 1.2.2 Sustainable larval control ........................................................................... 26 1.2.3 Larval control by autodissemination of pyriproxyfen ............................... 29 1.3 Insect Development and Reproduction Hormones ............................................. 30 1.3.1 Insect Growth Regulators .......................................................................... 31 1.3.2 Mechanism of action of Juvenile Hormone Analogues ............................. 32 1.4 Pyriproxyfen for control of mosquito vectors and other pests ........................... 33 5 1.4.1 Effect of pyriproxyfen on non-targeted organisms .................................... 36 1.4.2 Potential for pyriproxyfen to impact on malaria transmission ................... 37 1.4.3 Evolution of resistance
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